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Fiez, J. A.

Publications and source records attributed to Fiez, J. A..

9 recordsLinked to original sources

Reduced Dependence on Sensorimotor Processing in the Brain is Associated with Higher Math Skills in Adults

Number processing is crucial for math competence, yet the neural underpinnings remain unclear. In this study, we used functional magnetic resonance imaging (fMRI) to 1) identify key brain regions involved in symbolic and embodied number processing, and 2) examine their relations with math abilities in children and adults. We collected fMRI data from 104 adults (Mage = 23.25 years) and 88 4th graders (Mage = 9.75) as they performed number comparison and phonological tasks with numeral (symbolic) and hand (embodied) numerical stimuli. Participants math abilities were assessed using the math subtests of the Woodcock-Johnson Tests of Achievement. Univariate analyses revealed number processing regions in occipital, parietal and temporal cortices including inferior parietal, sensorimotor, supramarginal and insular areas. In adults, less involvement of sensorimotor processing regions during number compared to phonological processing is associated with enhanced math skills. These findings not only elucidate the neural mechanisms underlying number processing and math abilities but also raise questions about the emphasis on embodied number presentation in math learning experiences. Significance StatementChildren and adults show substantial individual differences in math competence, and understanding the underlying neural mechanisms is crucial. By employing functional magnetic resonance imaging (fMRI), we identified key brain regions involved in symbolic and embodied number processing and explored their relations with math skills. Our findings reveal that reduced sensorimotor involvement during number processing correlates with enhanced math performance in adults. This study not only elucidates the neural mechanisms underlying number processing, offering critical insights into the cognitive architecture that supports math abilities, but also raises questions about the emphasis on embodied number representations in math learning experiences.

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Subthalamic nucleus neurons encode syllable sequence and phonetic characteristics during speech

Speech is a complex behavior that can be used to study unique contributions of the basal ganglia to motor control in the human brain. Computational models suggest that the basal ganglia encodes either the phonetic content or the sequence of speech elements. To explore this question, we investigated the relationship between phoneme and sequence features of a spoken syllable triplet and the firing rate of subthalamic nucleus (STN) neurons recorded during the implantation of deep brain stimulation (DBS) electrodes in individuals with Parkinsons disease. Patients repeated aloud a random sequence of three consonant-vowel (CV) syllables in response to audio cues. Single-unit extracellular potentials were sampled from the sensorimotor STN; a total of 227 unit recordings were obtained from the left STN of 25 subjects (4 female). Of these, 113 (50%) units showed significant task-related increased firing and 53 (23%) showed decreased firing (t-test relative to inter-trial period baseline, p<0.05). Linear regression analysis revealed that both populations of STN neurons encode phoneme and sequence features of produced speech. Maximal phoneme encoding occurred at the time of phoneme production, suggesting efference copyor sensory-related processing, rather than speech motor planning (-50ms and +175ms relative to CV transition for consonant and vowel encoding, respectively). These findings demonstrate that involvement of the basal ganglia in speaking includes separate single unit representations of speech sequencing and phoneme selection in the STN.

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Speech induces spatiotemporal and frequency specific subthalamic-cortical spike-phase coupling events

Speech provides a rich context for understanding how cortical interactions with the basal ganglia contribute to unique human behaviors, but opportunities for direct intracranial recordings across cortical-basal ganglia networks are rare. We recorded electrocorticographic signals in the cortex synchronously with single units in the basal ganglia during awake neurosurgeries where subjects spoke syllable repetitions. We discovered that individual STN neurons have transient (200ms) spike-phase coupling (SPC) events with multiple cortical regions. The spike timing of STN neurons was coordinated with the phase of theta-alpha oscillations in the posterior supramarginal and superior temporal gyrus during speech planning and production. Speech sound errors occurred when this STN-cortical interaction was delayed. Our results suggest that the STN supports mechanisms of speech planning and auditory-sensorimotor integration during speech production that are required to achieve high fidelity of the phonological and articulatory representation of the target phoneme. These findings establish a framework for understanding cortical-basal ganglia interaction in other human behaviors, and additionally indicate that firing-rate based models are insufficient for explaining basal ganglia circuit behavior.

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Multiple adjoining word and face selective regions in ventral temporal cortex exhibit distinct dynamics

The map of category-selectivity in human ventral temporal cortex (VTC) provides organizational constraints to models of object recognition. One important principle is lateral-medial response biases to stimuli that are typically viewed in the center or periphery of the visual field. However, little is known about the relative temporal dynamics and location of regions that respond preferentially to stimulus classes that are centrally viewed, like the face- and word-processing networks. Here, word- and face-selective regions within VTC were mapped using intracranial recordings from 36 patients. Partially overlapping, but also anatomically dissociable patches of face- and word-selectivity were found in VTC. In addition to canonical word-selective regions along the left posterior occipitotemporal sulcus, selectivity was also located medial and anterior to face-selective regions on the fusiform gyrus at the group level and within individual subjects. These regions were replicated using 7 Tesla fMRI in healthy subjects. Left hemisphere word-selective regions preceded right hemisphere responses by 125 ms, potentially reflecting the left hemisphere bias for language; with no hemispheric difference in face-selective response latency. Word-selective regions along the posterior fusiform responded first, then spread medially and laterally, then anteriorally. Face-selective responses were first seen in posterior fusiform regions bilaterally, then proceeded anteriorally from there. For both words and faces, the relative delay between regions was longer than would be predicted by purely feedforward models of visual processing. The distinct time-courses of responses across these regions, and between hemispheres, suggest a complex and dynamic functional circuit supports face and word perception. Significance StatementRepresentations of visual objects in the human brain have been shown to be organized by several principles, including whether those objects tend to be viewed centrally or peripherally in the visual field. However, it remains unclear how regions that process objects that are viewed centrally, like words and faces, are organized relative to one another. Here, invasive and non-invasive neuroimaging suggests there is a mosaic of regions in ventral temporal cortex that respond selectively to either words or faces. These regions display differences in the strength and timing of their responses, both within and between brain hemispheres, suggesting they play different roles in perception. These results illuminate extended, bilateral, and dynamic brain pathways that support face perception and reading.

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Neutral auditory words immediately followed by painful electric shock show reduced next-day recollection

In this study, we investigated the effect of experimentally delivered acute pain on explicit and implicit memory. Twenty-five subjects participated in experimental sessions on consecutive days. The first session involved a categorization task intended to induce incidental memory encoding. There were two conditions, presented in randomized order, in which subjects listened to a series of words, which was repeated three times. In one condition, one-third of the word items were immediately followed by a painful electrical shock and these pain-paired items were presented unpredictably. In the other condition, all word items were not associated with pain. Response times over these repeated presentations were assessed for differences. Explicit memory was tested the following day, employing a Remember-Know assessment of word recognition, with no shocks employed. Recollection was significantly reduced for pain-paired words, as the proportion of correct Remember responses (out of total correct responses) was significantly lower. There were no significant reductions in memory for non-pain items that followed painful stimulation after a period of several seconds. Consistent with the experience of pain consuming working memory resources, we theorize that painful shocks interrupt memory encoding for the immediately preceding experimental items, due to a shift in attention away from the word item.

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Subthalamic nucleus and sensorimotor cortex activity during speech production

The sensorimotor cortex is somatotopically organized to represent the vocal tract articulators, such as lips, tongue, larynx, and jaw. How speech and articulatory features are encoded at the subcortical level, however, remains largely unknown. We analyzed local field potential (LFP) recordings from the subthalamic nucleus (STN) and simultaneous electrocorticography recordings from the sensorimotor cortex of 11 patients (1 female) with Parkinsons disease during implantation of deep brain stimulation (DBS) electrodes, while patients read aloud three-phoneme words. The initial phonemes involved either articulation primarily with the tongue (coronal consonants) or the lips (labial consonants). We observed significant increases in high gamma (60-150 Hz) power in both the STN and the sensorimotor cortex that began before speech onset and persisted for the duration of speech articulation. As expected from previous reports, in the sensorimotor cortex, the primary articulator involved in the production of the initial consonant was topographically represented by high gamma activity. We found that STN high gamma activity also demonstrated specificity for the primary articulator, although no clear topography was observed. In general, subthalamic high gamma activity varied along the ventral-dorsal trajectory of the electrodes, with greater high gamma power recorded in the more dorsal locations of the STN. These results demonstrate that articulator-specific speech information is contained within high gamma activity of the STN, with similar temporal but less specific topographical organization, compared to similar information encoded in the sensorimotor cortex.\n\nSIGNIFICANCE STATEMENTClinical and electrophysiological evidence suggests that the subthalamic nucleus is involved in speech, however, this important basal ganglia node is ignored in current models of speech production. We previously showed that subthalamic nucleus neurons differentially encode early and late aspects of speech production, but no previous studies have examined subthalamic functional organization for speech articulators. Using simultaneous local field potential recordings from the sensorimotor cortex and the subthalamic nucleus in patients with Parkinsons disease undergoing deep brain stimulation surgery, we discovered that subthalamic nucleus high gamma activity tracks speech production at the level of vocal tract articulators, with high gamma power beginning to increase prior to the onset of vocalization, similar to cortical articulatory encoding.

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The left midfusiform gyrus interacts with early visual cortex and the anterior temporal lobe to support word individuation.

The left mid-ventral temporal cortex (lmVTC) plays a dynamic role in reading. In this study we investigated the neural interactions that influence lmVTC dynamics and the lexical information these interactions are dependent on. We monitored activity with either intracranial electroencephalography or magnetoencephalography while participants viewed real words, pseudowords, consonant strings, and false fonts. A coarse level representation in early lmVTC activity allowed for decoding of visually dissimilar real words, pseudowords, and false fonts. Functional interactions between anterior ventral temporal regions, possibly containing stored knowledge about words, and low-order visual regions occurred after this initial stage of processing and was followed by the individuation of orthographically similar real words in lmVTC, but not similar pseudowords, letter strings, or false fonts. These results suggest that the individuation of real word representations in lmVTC is catalyzed by stored knowledge about word forms that emerges from network-level interactions with anterior regions of the temporal lobe.

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Memory for non-painful auditory items is influenced by whether they are experienced in a context involving painful electrical stimulation

In this study, we sought to examine the effect of pain on memory. Subjects heard a series of words and made categorization decisions in two different contexts. One context included painful shocks administered just after presentation of some of the words; the other context involved no shocks. For the context that included painful stimulations, every other word was followed by a shock and subjects were informed to expect this pattern. Word lists were repeated three times within each context in randomized order, with different category judgments but consistent pain-word pairings. After a brief delay, recognition memory was assessed. Non-pain words from the pain context were less strongly encoded than non-pain words from the completely pain-free context. An important accompanying finding is that response times to repeated experimental items were slower for non-pain words from the pain context, compared to non-pain words from the completely pain-free context. This demonstrates that the effect of pain on memory may generalize to non-pain items experienced in the same experimental context.

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Subthalamic nucleus neurons differentially encode early and late aspects of speech production

Basal ganglia-thalamocortical loops mediate all motor behavior, yet little detail is known about the role of basal ganglia nuclei in speech production. Using intracranial recording during deep brain stimulation surgery, we tested the hypothesis that the firing rate of subthalamic nucleus neurons is modulated in response to both planning and motor execution aspects of speech. Nearly half of 79 recorded units exhibited firing rate modulation, during a syllable reading task administered in 12 subjects. Trial-to-trial timing of changes in subthalamic neuronal activity, relative to cue onset versus production onset, revealed that locking to cue presentation was associated more with units that decreased firing rate, while locking to speech onset was associated more with units that increased firing rate. These uniquely acquired data indicate that subthalamic activity is dynamic during the production of speech, reflecting temporally-dependent inhibition and excitation of separate populations of subthalamic neurons.

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